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Title: A Constitutive Shade-Avoidance Mutant Implicates TIR-NBS-LRR Proteins in Arabidopsis Photomorphogenic Development

Author
item FAIGON-SOVERNA, ANA - U BUENOS AIRES ARGENTINA
item Harmon, Frank
item STORANI, LEONARDO - U BUENOS AIRES ARGENTINA
item KARAYEKOV, ELIZABETH - U BUENOS AIRES ARGENTINA
item STANELONI, ROBERTO - IIB-LELOIR BUENOS AIRES
item GASSMANN, WALTER - U MISSOURI COLUMBIA MO
item MAS, PALOMA - CSIC-IRTA BARCELONA SPAIN
item CASAL, JORGE - U BUENOS AIRES ARGENTINA
item KAY, STEVE - SCRIPPS INST LAJOLLA CA
item YANOVSKY, MARCELO - U BUENOS AIRES ARGENTINA

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/26/2006
Publication Date: 11/17/2006
Citation: Faigon-Soverna, A., Harmon, F.G., Storani, L., Karayekov, E., Staneloni, R.J., Gassmann, W., Mias, P., Casal, J.J., Kay, S.A., Yanovsky, M.J. 2006. A Constitutive Shade-Avoidance Mutant Implicates TIR-NBS-LRR Proteins in Arabidopsis Photomorphogenic Development. The Plant Cell 18(11):2919-2928.

Interpretive Summary: In plants, light signals caused by the presence of neighbors accelerate stem growth, flowering, and induce a more erect position of the leaves, a developmental strategy known as shade-avoidance syndrome. In addition, mutations in the photoreceptors that mediate shade-avoidance responses, primarily the red light photoreceptor phytochrome B (phyB), enhance disease susceptibility in Arabidopsis thaliana. This work reports a novel Arabidopsis mutant, named constitutive shade-avoidance 1 (csa1), which shows a shade-avoidance phenotype in the absence of shade and enhanced growth of a bacterial pathogen following infection. The causative mutation in csa1 is a dominant negative mutation resulting from enhanced expression of a truncated version of the normal CSA1 message, which produces aberrant phyB signaling. The CSA1 gene encodes for a Toll/Interleukin1 receptor-nucleotide binding site-leucine-rich repeat (TIR-NBS-LRR) protein. TIR-NBS-LRR proteins are a large class of proteins, which are mainly known to be involved in plant defense. This is the first report of a plant TIR-NBS-LRR protein acting outside of this paradigm. RPS4, the closest homologue of CSA1 in Arabidopsis, confers resistance to the bacterial pathogen Pseudomonas syringae. Interestingly, increasing the expression level of RPS4 complements the csa1 mutant phenotype; thus, responses to pathogens and neighbors share core-signaling components in Arabidopsis. These findings support previous data that suggest crosstalk between light signaling and defense responses. TIR-NBS-LRR proteins in animals (i.e., Drosophila melanogaster and Caenorhabditis elegans) are implicated in both development and immunity. Therefore, this work points toward a conserved function for TIR-domain proteins, which is shared across kingdoms, and suggests an ancient evolutionary origin for these receptors.

Technical Abstract: In plants, light signals caused by the presence of neighbors accelerate stem growth, flowering, and induce a more erect position of the leaves, a developmental strategy known as shade-avoidance syndrome. In addition, mutations in the photoreceptors that mediate shade-avoidance responses enhance disease susceptibility in Arabidopsis (Arabidopsis thaliana). Here we describe the Arabidopsis constitutive shade-avoidance 1 (csa1) mutant, which shows a shade-avoidance phenotype in the absence of shade and enhanced growth of a bacterial pathogen. The csa1 mutant has a T-DNA inserted within the second exon of a Toll/Interleukin1 receptor-nucleotide binding site-leucine-rich repeat (TIR-NBS-LRR) gene, which leads to the production of a truncated mRNA. Arabidopsis plants transformed with the truncated TIR-NBS-LRR gene recapitulate the mutant phenotype, indicating that csa1 is a dominant negative mutation that interferes with phytochrome signaling. TIR-NBS-LRR proteins had been implicated in defense responses in plants. RPS4, the closest homologue of CSA1, confers resistance to Pseudomonas syringae and complements the csa1 mutant phenotype, indicating that responses to pathogens and neighbors share core-signaling components in Arabidopsis. In Drosophila melanogaster and Caenorhabditis elegans TIR-domain proteins are implicated in both development and immunity. Thus, the dual role of the TIR-domain is conserved across kingdoms.